Diagnosis of nut-cracker phenomenon using renal Doppler ultrasound in orthostatic proteinuria
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1 Nephrol Dial Transplant 2001) 16: 1620±1625 Original Article Diagnosis of nut-cracker phenomenon using renal Doppler ultrasound in orthostatic proteinuria Byoung-Soo Cho 1, Young-Mi Choi 1, Hyeon-Ho Kang 1,SeongJinPark 2,JooWonLim 2 and Tai Young Yoon 3 Department of 1 Pediatrics, 2 Radiology, and 3 Preventive Medicine, College of Medicine, Kyung Hee University, Seoul, Korea Abstract Background. We evaluated the ef cacy of non-invasive renal Doppler ultrasound US) to detect the nutcracker phenomenon NCP) and we studied the prevalence of NCP in children with orthostatic proteinuria. Methods. Among a total 66 cases of orthostatic proteinuria, 39 cases of NCP were found, with 27 cases being detected in a normal control group. Using Doppler US, the anteroposterior AP) diameter and peak velocity PV) of the left renal vein LRV) were measured at the hilar and aortomesenteric portion. We calculated the ratio of AP and PV diameters between the two portions. The parameters were analysed using Student's t-test. Results. The AP diameters and the ratio in the hilar and narrow portions were all signi cantly different between the two groups P-0.01). The PV in the narrow portion and the ratio of PV were signi cantly different P-0.01), but the PV in the hilar portion was not statistically different between the two groups P)0.05). If the diagnostic criteria for NCP was that the ratio of PV was more than 5, then 22 subjects 56.4%) in the orthostatic proteinuria group and none in the control groupcould be diagnosed as NCP. If, however, the cut-off values for the diagnosis of NCP were set at the mean"2 SD of the ratio PV ratio 3.98 and size ratio 4.16), then the orthostatic proteinuria groupshowed abnormal AP diameter in %), peak velocity in %), and both in 21 patients 53.8%), and the control group showed an abnormal AP diameter in one subject 3.7%). Conclusions. NCP may be one of the leading causes of orthostatic proteinuria, and non-invasive renal Doppler US may be a useful diagnostic tool in the screening of NCP. In the future, the diagnostic criteria of NCP must be rede ned in children. Correspondence and offprint requests to: Byoung-Soo Cho MD PhD, Department of Pediatrics, College of Medicine, Kyung-Hee University Hospital, #1 Hoegi-dong Dongdaemun-ku, Seoul, Korea. Keywords: nut-cracker phenomenon; orthostatic proteinuria; renal Doppler ultrasound Introduction Compression of the left renal vein LRV) between aorta and superior mesenteric artery SMA), resulting haematuria, ank pain, varicocele, etc. is termed `nut-cracker phenomenon' NCP) or `left renal vein entrapment syndrome'. In the past invasive venography has been used for the diagnosis of NCP, but recently non-invasive methods such as computed tomography CT), ultrasound US), and magnetic resonance imaging MRI), etc. have been used more frequently. Most of the studies were performed in cases of haematuria. As yet, no large studies have been reported in orthostatic proteinuria. The purpose of this study is to assess the utility of renal Doppler US for the diagnosis of NCP in children. We also investigated the prevalence of NCP among patients with orthostatic proteinuria. Subjects and methods Subjects From the years 1997 to 1999 we evaluated 39 cases of NCP in an orthostatic proteinuria group, who were followed for at least 3 months, and who manifested normal BUN, creatinine, and blood pressure. Also, a normal control group 28 cases) with no evidence of renal disease or other chronic diseases were selected. We diagnosed subjects as having orthostatic proteinuria by the following criteria: no proteinuria in the early morning urine by dipstick test, more than 2q proteinuria by dipstick test in the daytime urine, and less than 1 g of proteinuria in 24-h collected urine. In the orthostatic proteinuria group, male : female ratio was 1.1 : 1 and mean age was 11 6±16) years. No subjects had haematuria by dipstick test. In the control group, male : female ratio was 0.9 : 1 and mean age was 10 6±16) # 2001 European Renal Association±European Dialysis and Transplant Association
2 Diagnosis of nut-cracker phenomenon using renal Doppler US years. There were no statistically signi cant differences between the groups. Methods After having fasted for 6±8 h, the patients ingested 150±300 ml tap-water 15±30 min before the US examination; US was then carried out using HDI 3000 with 7±4 and 4±2 MHz convex transducers and with the subjects supine. In the early part of this study we tried to obtain data in two positions, supine and upright. However, we could not obtain sonographic data in the upright position, because bowel gas interfered with sonographic examination of the left renal vein. Therefore, we obtained sonographic data only in the supine position. We calculated the mean of each parameter in each patient. We measured each parameter three times. Anteroposterior AP) diameter and peak velocity PV) were measured three times at two points in the LRV, one at the lateral portion of the LRV near the hilum, and the other as the LRV courses between the aorta and the SMA aortomesenteric portion). PV was measured in the transverse and longitudinal planes. The diameter of the LRV was measured with callipers at two points on grey-scale US, and the Doppler angle was kept at less than 608 Figures 1 and 2). All of the US examinations and interpretations of images were performed by two radiologists using the same methods. We obtained sonographic data in a blinded manner, not knowing whether the subjects had orthostatic proteinuria or were normal control subjects. Statistics We calculated the absolute values of the LRV as well as the ratio of PV and AP diameter between the two measured points, and compared the orthostatic proteinuria group with the control group. We performed statistical analysis with Student's t-test, using SPSS, and analysed correlations between the ratio of PV and AP diameter of the LRV in the orthostatic proteinuria group with Pearson's correlation coef cient. The mean " 2 SD of ratio of AP diameter and PV of the LRV between aortomesenteric and hilar portions was calculated for normal controls, and was used as the cut-off value for diagnosing NCP. We also analysed the proportion of NCP in the orthostatic proteinuria group. Results 1621 The mean AP diameter of the LRV in the orthostatic proteinuria group was 7.60 mm in the hilar area, 1.66 mm in the narrow portion, and the mean ratio of AP diameter was In contrast, the mean diameter of the LRV in the normal control groupwas 6.13 mm in the hilar area, 2.35 mm in the narrow portion, and the mean ratio of AP diameter was 2.77 mm. Between the two groups, the AP diameter in the hilar and narrow portions and the ratio of diameter were all signi cantly different P-0.01) Table 1, Figure 3). The results of peak velocity of LRV were that the mean PV of the orthostatic proteinuria group was cmus in the hilar area and cmus in the narrow portion, and the mean ratio of PV was In the normal control group, the results were cmus, cmus, and 2.57 respectively. The PV in the narrow portion and the ratio of PV were signi cantly different between the two groups P-0.01), but the PV in the hilar portion were not statistically different P)0.05) Table 2, Figure 4). According to some authors, if the diagnostic criteria for NCP was that the peak velocity ratio is more than 5 w4x, 22 cases 56.4%) in the orthostatic proteinuria groupand no cases in control groupwould have been Fig. 1. Using Doppler US, peak velocity of the left renal vein in the hilar portion measured 19.9 cmus.
3 1622 B.-S. Cho et al. Fig. 2. The velocity of the left renal vein in the narrow portion was cmus; it was six times faster in the hilar portion. Table 1. The AP diameter of the LRV between the two groups Table 2. The peak velocity PV) of the LRV between the two groups Orthostatic proteinuria Control P value Orthostatic proteinuria Control P value Hilar size mm) 7.60" " Narrow portion size* 1.66" " Size ratio 5.50" " Hilar PV cmus) 19.88" "2.81 )0.05 Narrow portion PV " " PV ratio 5.52" " * Narrow portion: aortomesenteric portion. Fig. 3. The ratio of AP diameter between hilar and aortomesenteric portions. diagnosed as NCP. However, if the cut-off value for the diagnosis of NCP were set at the mean"2 SD PV ratio 3.98, size ratio 4.16 ), the orthostatic proteinuria groupshowed an abnormal AP diameter in %), Fig. 4. The ratio of PV between the hilar and aortomesenteric portions. PV in %), and both in 21 patients 53.8%), and the control groupshowed an abnormal AP diameter in one subject 3.7%) Table 3). We analysed the orthostatic proteinuria group with Pearson's correlation coef cient and there were
4 Diagnosis of nut-cracker phenomenon using renal Doppler US Table 3. The diagnostic criteria of NCP Cut-off value signi cant correlations between the ratio of the PV and the AP diameter rs0.776, Ps0.000) Figure 5). Discussion Orthostatic proteinuria number %) Control number %) PV ratio) %) 0 )mean"2 SD 3.98) %) 0 AP diameter) %) 0 )mean"2 SD 4.16) %) 1 3.7%) Both %) 0 Fig 5. Correlation between the ratio of PV and AP diameter rs0.776). The prevalence of asymptomatic proteinuria differs greatly between reports, and ndings of 0.6 ±10.7% w1,2x have been published. Asymptomatic proteinuria may result in renal dysfunction if underlying disease is present and must be followed up carefully. However, half of all cases of asymptomatic proteinuria is due to orthostatic proteinuria, which is a benign condition, and no treatment is necessary because it does not progress to renal failure. The mechanism of orthostatic proteinuria is not yet clearly de ned. Shintaku et al. w3x proposed a partial obstruction to the ow in the LRV. Vehaskari w4x suggested that a mechanism consisting of both an underlying subclinical immune injury and a superimposed exaggerated haemodynamic response would resolve many of the discrepancies. Under this hypothesis, the subtle glomerular injury would not by itself cause protein excretion, or at most would increase it only minimally, and the additional haemodynamic stress of elevated glomerular intracapillary pressure 1623 mediated by angiotensin II) in the upright posture would be required to produce frank proteinuria w4x. Other hypotheses focus on a `renal congestion' theory. Kelling w5x proposed that the erect posture could close the angle between the aorta and SMA, leading to compression of the LRV and renal congestion. Buchanec et al. w6x observed that renal ptosis was more common in children with orthostatic proteinuria, and emphasized that angling of the renal vein would bring about passive renal congestion. This `renal congestion' theory of orthostatic proteinuria is very similar to the mechanism of NCP w3,7x. NCP was rst described in 1972 by De Schepper w8x, and results from compression of the LRV between the aorta and the SMA. The phenomenon is manifested by gross haematuria or microscopic haematuria, left ank pain, varicocele, gonadal vein engorgement, etc. The haematuria may result from increased LRV pressure causing minute rupture of thin-walled veins into the collecting systems or calyceal fornix w9x or communication between dilated venous sinuses and adjacent renal calyces w10x. NCP is a benign condition and if the symptoms are mild, no treatment is necessary. If clinical symptoms are severe, operative treatment such as medial nephropexy with excision of renal varicosities w11x, renal-vein bypass w12x, autotransplantation w13x, etc. should be considered. The mechanism of NCP is unknown. NCP is generally more severe in the erect posture than in the supine position, owing to visceral ptosis or pressure gradients. It is not clear why compression of the vein occurs in some patients. Shintaku et al. w3x reported that 15 patients with orthostatic proteinuria had entrapment of the LRV by the aorta and SMA, and the NCP may possibly be a cause of moderate to massive orthostatic proteinuria. Lee et al. w7x also reported two NCP patients with orthostatic proteinuria. We were interested in this point and investigated the prevalence of NCP among the orthostatic proteinuria group. Our data showed a de nite difference in results between the orthostatic proteinuria group and the normal control group. We supposed that by `renal congestion', orthostatic proteinuria and NCP can develop in the same patient, and NCP may cause orthostatic proteinuria. But our study has some limitations, because we did not examine renal venography, and renal Doppler could not con rm our diagnosis. In addition, because the number of cases was so small, we could not ignore statistical errors. For the diagnosis of NCP, several diagnostic tools are applied, but de nite diagnostic criteria have not yet been established. The widely used diagnostic method of NCP is renal venography. Ekim et al. w14x report a rarer pattern of this phenomenon, so-called posterior nutcracker, as the cause of orthostatic proteinuria. They performed a selective venography and aortography and con rmed the presence of a markedly compressed LRV between the aorta and the luminal vertebral body proximal to the insertion into the inferior vena cava. The cut-off value of
5 1624 B.-S. Cho et al. differences of pressure between aortomesenteric and hilar portions is proposed as more than 3 mmhg w2,15,16x. However, these criteria have sometimes led to a misdiagnosis of NCP because some children normally have a narrow LRV. Some have tried non-invasive rather than invasive screening methods angiographic CT w17x, MRI w18x, Doppler US w19±21x, etc). Doppler sonography can provide physiological information about blood ow in the LRV. Kim et al. w20x reported that the measurement of diameter and peak ow velocity in both distal and proximal portions of the LRV is useful for diagnosis of NCP. According to their study, a ratio of AP diameter and PV greater than 5.0 should be the cut-off level for the syndrome. Applying this criterion, sensitivity was 80%, speci city 94%, and accuracy 83% w20x, but there was controversy in regard to the criteria. We agree that there are some problems using US for the diagnosis of NCP, but Doppler US is a simple and non-invasive method. For example, measurement of the diameter and the PV of the LRV can vary between operators, and sometimes the image is dif cult to obtain because of intestinal gas. Moreover, it is dif cult to measure the narrow portion of the PV in children because the sampling area of the LRV is too small and the Doppler angle is larger than in adults, due to the almost horizontal left renal venous ow into the inferior vena cava after the narrow portion. Therefore, very few data have been reported in children and the criteria of childhood NCP has not been established. If the ow velocity can be calculated in the narrow portion of the LRV in children, the Doppler sonographic instrument will become a powerful tool for the diagnosis of NCP. In our study, it was not dif cult to obtain a Doppler spectrum sampling from the left renal vein. Although our number of cases was small, we could obtain Doppler US data in nearly all cases. Our data showed that values are signi cantly different between the two groups, except for PV in the hilar portion of the LRV. If the criteria for the diagnosis of NCP is a PV ratio of more than 5, anduor the ratio of AP diameter is more than 5, there would be 53±56% cases of NCP in our orthostatic proteinuria group, but none in our normal control group. These signi cant differences are indirect proof that orthostatic proteinuria may be caused by renal congestion resulting from compression of the LRV and that NCP may be one of the common causes of orthostatic proteinuria, because the US nding in our orthostatic proteinuria group t into the criteria for the diagnosis of NCP. There are some questions as to why the combined haematuria and proteinuria conditions are not more frequent, and why isolated symptoms are more frequently observed. In addition, there is confusion about the criteria of NCP when using Doppler US. The mean " 2 SD of ratio may be different between children and adults. Therefore, we think that a larger number of cases must be studied and the mean"2 SD data should be obtained. The criteria of the ratio of AP diameter and PV of more than 5 has been preferred until now. If the data is obtained, it can be used as the criteria for NCP, and Doppler US will become a powerful diagnostic tool in the diagnosis of NCP. In conclusion, NCP might be one of the leading causes of orthostatic proteinuria, and non-invasive renal Doppler US may be a useful diagnostic tool in the screening of NCP. The diagnostic criteria of NCP in children by Doppler US should be rede ned. Acknowledgements. The authors would like to thank Mrs A. Alice for her secretarial support and proof-reading. An abstract of this article was presented at the poster section of 34th ESPN in Helsinki, Finland. References 1. Beinart C, Sniderman KW, Tamura S, Vaughan ED, Sos TA. Left renal vein into inferior vena cava pressure relationship in humans. J Urol 1981; 127: 1070± Nishimura Y, Fushiki M, Yoshida M et al. Left renal vein hypertension in patients with left renal bleeding of unknown origin. Radiology 1986; 160: 663± Shintaku N, Takahashi Y, Akaishi K, Sano A, Kuroda Y. Entrapment of left renal vein in children with orthostatic proteinuria. Pediatr Nephrol 1990; 4: 324± Vehaskari VM. Mechanism of orthostatic proteinuria. Pediatr Nephrol 1990; 4: 328± Kelling G. Zur Frage der orthostatischen Albuminurie. Zentralbl Inn Med 1919; 40: 313± Buchanec J, Kliment J, Javorka K, Belakova S. X-ray changes in the kidneys of children with orthostatic proteinuria. Int Urol Nephrol 1983; 15: 3±9 7. Lee SJ, You ES, Lee JE, Chung EC. Left renal vein entrapment syndrome in two girls with orthostatic proteinuria. Pediatr Nephrol 1997; 11: 218± De Schepper A. 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Intra-arterial digital subtraction angiography for children with idiopathic renal bleeding: a diagnosis of nutcracker phenomenon. Clin Nephrol 1988; 30: 134± Sacks BA, Gomori J, Lerner M, Master R. Left renal hypertension in association with the nutcracker phenomenon. Cardiovasc Intervent Radiol 1981; 4: 253± Shokeir AA, el-diasty TA, Ghoneim MA. The nutcracker syndrome: new methods of diagnosis and treatment. Br J Urol 1994; 74: 139± Hohenfellner M, Steinbach F, Schultz-Lampel D et al. The nutcracker syndrome: New aspect of pathophysiology, diagnosis and treatment. J Urol 1991; 146: 685± Takebayashi S, Ueki T, Ikeda N, Fujikawa A. Diagnosis of the NCP with color Doppler sonography. AJR 1999; 172: 39±43
6 Diagnosis of nut-cracker phenomenon using renal Doppler US 20. Kim SH, Cho SW, Kim HD, Chung JW, Park JH, Han MC. Nutracker syndrome: Diagnosis with Doppler US. Radiology 1996; 198: 93± Stavros AT, Sickler KJ, Menter RR. Color duplex sonography of the nut-cracker syndrome aortomesenteric left renal vein compression). J Ultrasound Med 1994; 13: 569±574 Received for publication: Accepted for publication:
Citation 泌尿器科紀要 (1994), 40(2):
Title Nutcracker phenomenon: a case with diagnostic criteria Author(s) Ishidoya, Shigeto; Chiba, Yutaka; S Seiichi Citation 泌尿器科紀要 (1994), 40(2): 135-138 Issue Date 1994-02 URL http://hdl.handle.net/2433/115201
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